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Home , Antarctophthirus, Echinophthiriidae, South American sea lion

Parasitology Research (2019) 118:1353–1361 https://doi.org/10.1007/s00436-019-06273-2

ARTHROPODS AND MEDICAL ENTOMOLOGY - ORIGINAL PAPER

Antarctophthirus microchir infestation in synanthropic South American sea (Otaria flavescens) males diagnosed by a novel non-invasive method

David Ebmer1 & Maria José Navarrete2 & Pamela Muñoz2 & Luis Miguel Flores2 & Ulrich Gärtner3 & Anja Taubert1 & Carlos Hermosilla1

Received: 29 December 2018 /Accepted: 18 February 2019 /Published online: 14 March 2019 # The Author(s) 2019

Abstract microchir is a sucking species belonging to the family and has been reported to parasitize all species of the subfamily Otariinae, the sea . Former studies on this ectoparasite mainly required fixation, immobilization, or death of host species and especially examinations of adult male sea lions are still very rare. Between March and May 2018, adult individuals of a unique Burban^ bachelor group of South American sea lions (Otaria flavescens)living directly in the city of Valdivia, , were studied regarding their ectoparasite infestation status. For first time, a non-invasive method in the form of a lice comb screwed on a telescopic rod and grounded with adhesive tape was used for sample taking process. Overall, during combing different stages of A. microchir were detected in 4/5 O. flavescens individuals, especially at the junction between the back and hind flippers. Our findings represent the first report of A. microchir infesting individuals of this synanthropic colony and fulfilling complete life cycle in a group despite inhabiting freshwater and in absence of females/ pups. Our Btelescopic lice comb apparatus^ offers a new strategy to collect different stages of ectoparasites and a range of epidermal material, such as fur coat hair and superficial skin tissue for a broad spectrum of research fields in wildlife sciences in an unmolested and stress reduced manner.

Keywords Echinophthiriidae . Synanthropy . Urban sea lions . Non-invasive sampling

Introduction sucking lice (Durden and Musser 1994; Leonardi and Palma 2013), which represents a group of permanent, obligate, and Antarctophthirus microchir isamemberofthefamily wing-free ectoparasitic of eutherian Echinophthiriidae belonging to the suborder Anoplura, the exhibiting a hematophagous lifestyle (Kim and Ludwig 1978). Representatives of Echinophthiriidae are of special in- terest since they are the only sucking lice family which infest Section Editor: Boris R. Krasnov host species with semi-aquatic lifestyles, such as Pinnipedia Electronic supplementary material The online version of this article and American river ( canadensis)(Murray1976; (https://doi.org/10.1007/s00436-019-06273-2) contains supplementary Kim 1985;LeonardiandPalma2013). The host range of the material, which is available to authorized users. genus Antarctophthirus comprises different includ- ing the families , Otariidae, and Phocidae * David Ebmer (Leonardi and Palma 2013). Compared with the other six [email protected] host-specific members within the genus, A. microchir infests a broader range of host species. Thus, findings on this parasite 1 Institute of Parasitology, Biomedical Research Center Seltersberg were reported from all six species of the otariid subfamily (BFS), Justus Liebig University Giessen, Schubertstr. 81, 35392 Giessen, Germany Otariinae, the sea lions, which show a wide geographical dis- tribution and occur in both hemispheres (Kim et al. 1975; 2 Instituto de Patología , Facultad de Ciencias Veterinarias, Universidad Austral de Chile, Valdivia, Chile Leonardi and Palma 2013; Leonardi et al. 2014). Previous findings reported on A. microchir from free-ranging South 3 Institute of Anatomy and Cell Biology, Justus Liebig University Giessen, Aulweg 123, 35385 Giessen, Germany American sea lion (Otaria flavescens) pups from 1354 Parasitol Res (2019) 118:1353–1361 and included re-description (Leonardi et al. 2009), morpho- (i.e., hair, dandruffs, epidermal cells/debris, and ectoparasites) logical studies (Leonardi et al. 2012a) and numerous publica- without considerable disturbance. tions on biology (Leonardi et al. 2012b;LeonardiandLazzari 2014), transmission (Leonardi et al. 2013), and population dynamics (Aznar et al. 2009) of this parasite. First description Material and methods of A. microchir parasitizing O. flavescens in Chile was pub- lished in 2008 (Crovetto et al. 2008). Study area The South American sea lion shows a wide geographical occurrence commonly ranging along the Pacific coast of During March and May 2018, an Burban^ bachelor group of and Chile, the Atlantic coast of Southern Brazil, , South American sea lions (O. flavescens) was evaluated with- Argentina, and on the (Vaz-Ferreira 1982). in the Chilean city Valdivia for its ectoparasite infestation These polygynous marine mammals live in distinct social struc- status. The study area comprised different resting spots of this tures including harems or bachelor colonies (Cárdenas-Alayza colony at riverside piers and construction sites (39° 48′ 2017). The Chilean city Valdivia is located approximately 37.566″ S, 73° 14′ 49.289″ W), the local market (39° 15 km east of the Pacific Ocean and since the late 1970s this city 48′ 46.84″S, 73° 14′ 54.212″ W), and a swimming platform has been harboring a synanthropic bachelor group of (39° 48′ 46.988″ S, 73° 14′ 55.24″ W), all being located along O. flavescens (Schlatter 1976)—a unique Burban^ colony of or on the freshwater river Calle-Calle within a vicinity of sea lions, which represents the only colony worldwide perma- 4km2. nently living in a freshwater habitat. To date, this sea lion colony is composed of approximately 70 individuals between 2 and Non-invasive combing method 15 years of age which still exchange with the Pacific colonies. Their daily presence at the local fish market, a hot-spot of inter- In order to distinguish single individuals of the colony and to action between humans, sea lions, stray , , and birds, create a colony register, were observed by eye, indi- leads to a remarkable close contact between sea lions and inhab- vidually photographed (Sony Alpha 5100®, Minato, Japan; itants or domestic pets within the city of Valdivia. At the same Apple iPhone 8 Plus®, Cupertino, USA) and filmed by a time, this close contact enables transmission of different patho- camera drone (DJI Mavic Pro®, Shenzhen, China). For sam- gens. Consistently, a parasitological investigation on the endo- ple collection, a novel non-invasive combing apparatus was parasite fauna of this sea lion colony was carried out and several here designed: a metal-toothed lice comb, fabricated for do- protozoan and metazoan taxa bearing zoonotic potential [i.e., mestic pets (TRIXIE® Heimtierbedarf GmbH & Co. KG, Cryptosporidium, Giardia, Neobalantidium (former Tarp, Germany), bolted on an aluminum telescopic rod fixed Balantidium; Mathison and Pritt 2019), Diphyllobothriidae gen. with tape (TESA®, Norderstedt, Germany), was used for a sp., Anisakidae gen. sp.) were detected (Hermosilla et al. 2016a). broad spectrum of sea lion epidermal material collection In past decades, most investigations on echinophthiriid lice (i.e., fur coat hair, lice, nits, and skin tissue samples). The total required capturing and fixation techniques (Murray and length of Btelescopic lice comb apparatus^ was 1.75 m, the Nicholls 1965;Kim1972;Kim1975;Thompsonetal.1998; metal-teeth row of the comb was 7.5 cm, a single tooth mea- Mehlhorn et al. 2002; Crovetto et al. 2008; Leonardi et al. sured 1.5 cm in length and space between each tooth was 2012b), immobilization applying anesthetic protocols 0.5 mm (Fig. 1). (Murray and Nicholls 1965; Thompson et al. 1998;Dailey et al. 2005; Leonardi et al. 2014, 2016), or even death of Sample collection procedure free-ranging host species (Scherf 1963;Murrayand Nicholls 1965;Murrayetal.1965;Kim1972 ). Furthermore, For sampling, five non-aggressive sea lions (aged 11 years or several investigations were performed during necropsies of older) were chosen on the basis of trustfulness and individual found carcasses of O. flavescens individuals (Morgades et al. characteristics, i.e., significant skin alterations and apparent 2006; Gomez-Puerta and Gonzales-Viera 2015). pruritus, neoplasia and/or ophthalmic pathologies. When ap- For the first time, the current study delivers data on the proaching the animals, it was of top priority to radiate a sense ectoparasite fauna of the synanthropic colony of of calm and serenity and to maintain direct eye contact with O. flavescens from Valdivia, Chile, by using a self-designed the animals, thereby constantly avoiding frantic movements Btelescopic lice comb apparatus^ for non-invasive lice/nits and loud noises. It appeared beneficial to work from an ele- sample collection. This non-invasive technique is also appli- vated position or at least to stay at eye-level to the sea lions. cable for future monitoring projects on ectoparasite infesta- Depending on acceptance of individuals to humans, an inter- tions of other pinniped species [e.g., harbor seals ( space of at least 0.2–1.5 m was always kept. After selection of vitulina) and gray seals (Halichoerus grypus)] and might serve an individual, firstly the telescopic rod was carefully moved to acquire a wider range of valuable biological skin material into the vision field of the sea lion. Secondly, the sea lion was Parasitol Res (2019) 118:1353–1361 1355

video footage of the combing process reveals insights in this special kind of field work (Online Resource 1). Sea lion sampling was conducted in accordance with the Institutional Ethic Commission of the University Austral of Chile (Chile) and to the Justus Liebig University Giessen (Germany). Permission for sea lion sample collection within the city of Valdivia was extended by the Municipality Service of the city of Valdivia and the Chilean National Service of Fishing and Aquaculture (SERNAPESCA) and in accordance with current Chilean Animal Welfare Legislation.

Storage and morphological identification of A. microchir stages

Sucking lice stages were removed from the lice comb by using dissecting needles and transferred to ziplock bags (please see Fig. 2e and Online Resource 2). Thereafter, specimens were preserved in 70% ethanol and analyzed using a light micro- scope (Olympus CX31®, Shinjuku, Japan). For identification, morphological keys for family and genus level (Murray 1976; Kim 1987; Mehlhorn et al. 2002) and morphometric data of A. microchir (Leonardi et al. 2009)wereapplied.

Scanning electron microscopy

A female A. microchir preserved in 80% ethanol was used for scanning electron microscopy (SEM) analysis. Briefly, thespecimenwasgentlydepositedonacircular(10mm of diameter) glass coverslips (Nunc) pre-coated with

poly-L-lysine (Sigma-Aldrich). Thereafter, the sample was fixed in 2.5% glutaraldehyde (Merck), post-fixed in 1% osmium tetroxide (Merck), washed in distilled water, B ^ Fig. 1 Telescopic lice comb apparatus . Overview and close-up of the dehydrated, dried by CO treatment, and afterwards metal-toothed lice comb on the head of an aluminum telescopic rod fixed 2 with Tesa® tape sputtered with gold (Villagra-Blanco et al. 2017). The sample was examined by using a Philips XL30® (Amsterdam, Netherlands) scanning microscope equipped with a digital camera allocated at the Institute of Anatomy allowed to sniff, lick, and explore the combing tool. Then, and Cell Biology (Justus Liebig University Giessen, cautious initial skin contact was made and the individuals Germany). were first combed in anterior parts of their body, especially in regions of the head and neck (Fig. 2a–d).Incaseofaccep- tance, posterior parts of the body, dorsum, hind flippers, and Results pelage were also sampled. Reduced hand movements (e.g., showing palm of the hand) and soft-spoken words clearly Non-invasive combing procedure and microhabitats showed calming effects on sea lions’ behavior (see Fig. 2c, of A. microchir on O. flavescens body surface d). In addition, interactions were documented with a GoPro Hero 5® (San Mateo, USA) camera fixed on a headband Starting the combing process at anterior parts of the body, (Fig. 3). including the forehead, dorsal, and ventral areas of the neck, Important to note, animals submitted to sampling process was necessary to obtain the sea lion’s confidence. All other were never fed or lured with feed or any other reinforcement body areas were studied after cautious skin contact and a auxiliaries. By performing the sampling at open areas near phase of familiarization at cranial body parts. Considering this freshwater habitats, the animals always had the chance to chronological order, selected sea lions tolerated the combing leave at any time during the sampling process. Additional procedure very well and accepted human presence in the 1356 Parasitol Res (2019) 118:1353–1361

Fig. 2 Sampling of the synanthropic O. flavescens colony within the city of Valdivia. a, b Sampling from a boat while the sea lion is resting on a swimming platform on the river of Calle-Calle in front of the local fish market. c, d Sampling at a typical resting place of O. flavescens in Valdivia. e Lice comb after combing process, item full of hair, and skin tissue; in the background: dissection needle and ziplock bag for sample storage

middle of the colony (Fig. 2c, d). Recurrent defensive behav- younger animals could not be included in the sampling pro- ior hardly occurred during sampling. Due to natural shyness, cess. The total combing time (i.e., entire body, anterior, and

Fig. 3 GoPro view: area selection during sampling process on a swimming platform. a Application of the Btelescopic lice comb apparatus^. b Starting point of sampling process: anterior parts of the body to gain sea lion’s trust. c Consecutive sampling area: posterior parts of the body. d Curious members of the Burban^ sea lion colony watching the examination. e Local fish market in the background with numerous sea lions waiting for fish waste Parasitol Res (2019) 118:1353–1361 1357 posterior parts) varied between individuals and encompassed Microscopical findings between 15 and 45 min/individual and examination. Five sampled sea lions showed clear satisfaction while being Light microscopic examination of different stages (Fig. 4)and combed thereby extending their heads or necks, changing SEM analysis of a female specimen (Fig. 5a, b) allowed mor- position towards to telescope in order to accommodate cer- phological species identification of A. microchir according to tain areas of pruritus to the comb devise (please refer to literature (Enderlein 1906; Leonardi et al. 2009). The head of Online Resource 1). A. microchir was eyeless (Fig. 5a) and carried thick antennae Overall, all A. microchir stages were detected at the on both lateral sides. In adult lice, the antennae were com- caudal back of the animals, especially at the junction be- posed of five tapering segments (Fig. 4c, d), while the tween the back and the hind flippers (Fig. 3). The second- second-stage larva showed antennae with four segments stage larva was located near the flank, slightly more ven- (Fig. 4b). The genital opening of the female stage was laterally tral than the other stages. No stages of A. microchir were bordered with two clusters of hairs, which consisted of long found at cranial parts of sea lion’s body even though skin and slightly modified setae (Fig. 5b). Abdominal segments lesions were also apparent at these areas. Collected skin were coated with overlapping scales, which showed a typical samples consisted of hair, dandruffs, epidermal debris, flat, oval, and leaf-like shape (Fig. 5b). Spines exhibited a and ectoparasite stages. typical elongated shape with a tapering end and could clearly be distinguished from scales (Fig. 5b). Nomenclature of setae Infestation with A. microchir was guided by the description of Kim and Ludwig (1978)and additionally according to the revised published by Evaluation of the ectoparasite status of this synanthropic col- Mehlhorn et al. (2002) and Leonardi et al. (2009). ony revealed a patent infestation with the echinophthiriid louse A. microchir in 80% (4/5) of O. flavescens individuals. In total, nine adult A. microchir stages (three females and six Discussion males), 1 second-stage larva and three nits of A. microchir have been detected (Fig. 4). The presence of all these different Overall, ectoparasite studies on A. microchir in free-ranging stages proved that the entire lifecycle was completed on the South American sea lions generally focused so far on pups animals despite residing in a freshwater habitat and in the due to easier handling while capturing and fixation (Leonardi absence of females and pups. No other ectoparasite species et al. 2012b;Leonardi2014), whereas knowledge on infesta- were here identified. tion status of adult individuals, especially males is still very

Fig. 4 Light microscopic images of different stages of A. microchir. a Nit. b Second-stage larva. c Adult male. d Adult female. Scale bars, 500 μm 1358 Parasitol Res (2019) 118:1353–1361

Fig. 5 Scanning electron microscopic images of an adult female of A. microchir. View of a eyeless head and fivefold segmented antennae, b female genital porus surrounded by clusters of hairs (ha), leaf-like shaped scales (sc), and spines (sp). Scale bars, 100 μm

little (Crovetto et al. 2008). To our best knowledge, the ecto- protecting methods for obtaining a broad range of biological parasite infestation status of free-ranging bachelor colonies of material (Kleinertz et al. 2014; Hermosilla et al. 2015, 2016a, O. flavescens has never been examined before. b, 2018a, b). Taking advantage from a striking adaptation of this Burban^ Morphological characteristics of A. microchir were intensive- colony of South American sea lions to human activities, we ly studied in the past, and the morphological identification of the here developed a Btelescopic lice comb apparatus^ allowing current specimen was in accordance with published determina- for skin sampling of adult sea lions in a non-invasive and stress tion keys (Enderlein 1906;Murray1976;Kim1987;Mehlhorn reduced way. By obtaining biological material of pinnipeds, et al. 2002), the re-description (Leonardi et al. 2009), and SEM e.g., hair (including roots), skin tissue samples (e.g., dandruffs), examination of this species (Leonardi et al. 2012a). and different parasite stages, this method opens a broad spec- Regarding predilection sites of the genus Antarctophthirus, trum of new research fields and could support future projects, Kim (1975) reported eyelids, hips, hind flippers, and tail as including endocrinological (Koren et al. 2002; Sheriff et al. main body sites of sucking lice. However, Leonardi et al. 2011), toxicological (Castellini et al. 2012; McHuron et al. (2012b)failedtodetectA. microchir on hind flippers of pups 2012; Peterson et al. 2016), and even molecular genetic analy- and mainly found them on the back and the belly. Important to ses of sampled animals. Moreover, this method allows not only note, due to fixation, anterior parts of pup bodies were not unmolested sample collections, but also offers security mea- examined (Leonardi et al. 2012b). Another study reported sures by guaranteeing a certain interspace between researchers A. microchir to infest the basis of the snout (Crovetto et al. and animals. The non-invasive aspect of this method was also 2008). In contrast to other monoxenous lice genera, reflected by the choice of sampling spots. As such, each animal Antarctophthirus infests a wide range of host species, involving could interrupt examination and leave at any time the combing eared seals (Otariidae), (Odobenidae), and earless process. Since many individuals of this colony were cluttered seals (Phocidae) (Leonardi and Palma 2013), which may all with skin lesions (e.g., alopecia, hyperkeratosis, pruritus), differ in their mode of locomotion, pelage, and geographical which could also be caused by bacterial or fungal infections, distribution (Leonardi et al. 2012b). As already described for most animals cooperated very well and even seemed to enjoy the closely related chewing lice of chicken (Johnson et al. the treatment due to pruritus relief. This impression was 2012), it was discussed that Antarctophthirus infestation of cer- strengthened by the duration of the combing process, which tain areas of hosts may represent a microhabitat selection. lasted up to 45 min per individual. Enderlein (1906) suggested that in contrast to Echinophthirius However, despite their excellent adjustment to a life in the spp., which are characterized by the absence of scales and city, it has to be kept in mind that the current synanthropic sea mainly infest areas of seals head, the presence of scales in case lion population still represents wild and free-ranging animals of Antarctophthirus spp. could be essential for lice breathing (Schlatter 1976) and younger individuals can still migrate to activities in case that parts of the body related to respiration the Pacific colonies at reproductive ages. Consequently, the (e.g., head, snout) would not be infested. Consistently, in the sampling process delivers a smaller amount of biological ma- current study all stages of A. microchir were found in posterior terial and is more time consuming than examination of fixed parts of the body, especially at caudal parts of the back close to animals (Leonardi 2014) or during necropsies. However, in the junction to the hind flippers accordingly to Kim (1975). today’s world, where anthropogenic pressure influences and Different echinophtiriid lice transmission routes have been determines wildlife as intensive as never before, non-invasive reported, whereby all of them can only occur if the pinniped or minimally invasive methods should constitute indispens- host is ashore (Kim 1975). In case of Proechinophthirus able tools in research of marine mammals (Gales et al. fluctus and A. callorhini, parasitizing the Northern 2009), and it is in our responsibility to develop creative, (Callorhinus ursinus), Kim (1972) proposed direct Parasitol Res (2019) 118:1353–1361 1359 transmission from cows to pups, especially in first hours after Acknowledgments We would like to gratefully thank Rafael Burgos parturition, as the major pathway of transmission. Pup-to-pup (Institute of Pharmacology), Enrique Paredes (Institute of Pathology), and Javier Painean Peña (Institute of Parasitology) for the great assistance transmission of lice may also play a pivotal role, particularly at the Universidad Austral de Chile, Valdivia, Chile. Further we are thank- in crowded colonies (Kim 1975). In contrast, horizontal trans- ful to Esteban Reyes Lobao-Tello and Sandra Azócar for their kind help mission between cows and bulls was described as unlikely due during field studies as well as the Municipality Service of the city of to low lice densities on adult seals (Kim 1975). Indirect trans- Valdivia and SERNAPESCA for permission to enter and collect samples at construction areas. mission through lice/larval stages that have fallen from hosts have not been described so far but might occur as this trans- Funding This study was funded by the Institute of Parasitology (Justus mission route is well-known for closely terrestrial lice genera Liebig University Giessen) and the Institute of Pathology (Universidad (e.g., Haematopinus, Pediculus). In line to direct transmis- Austral de Chile). sion, cow-to-pup transmission was also confirmed as main transmission route for A. microchir under natural conditions Compliance with ethical standards (Aznar et al. 2009; Leonardi et al. 2013). Early stages of Sea lion sampling was conducted in accordance with the Institutional A. microchir, i.e., eggs and first larval stages, were reported Ethic Commission of the University Austral of Chile (Chile) and to the to mainly occur on pups, which avoid water contact during Justus Liebig University Giessen (Germany). Permission for sea lion their first weeks of life (Leonardi and Lazzari 2014). sample collection within the city of Valdivia was extended by the Consistently, in vitro experiments revealed that these lice Municipality Service of the city of Valdivia and the Chilean National Service of Fishing and Aquaculture (SERNAPESCA) and in accordance stages poorly tolerated periods underwater (Leonardi and with current Chilean Animal Welfare Legislation. Lazzari 2014), which is in accordance with weak water resis- tance of eggs revealed in other studies on echinophtiriid lice Conflict of interest The authors declare that they have no conflict of (Murray and Nicholls 1965). However, in contrast to first- interest. stage larvae, later larval stages and adults of A. microchir tol- erate periods of submersion (Leonardi and Lazzari 2014). Interestingly, the synanthropic O. flavescens population in Open Access This article is distributed under the terms of the Creative Valdivia exclusively consisted of male individuals, with the Commons Attribution 4.0 International License (http:// youngest members being aged approximately 2 years. The creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give fact that nits, second-stage larva, and adult lice (females and appropriate credit to the original author(s) and the source, provide a link males) were detected on these animals, proves that to the Creative Commons license, and indicate if changes were made. A. microchir is capable to fulfill the entire life cycle within this bachelor group even in the absence of pups, yearlings, or females. The ever-granted availability of fish at the local mar- ket may shorten or even occasionally cut the hunting periods of these animals thereby resulting in extended periods ashore. References Based on the distinct social behaviors of this synanthropic bachelor group, the animals exhibit longer circadian resting Aznar FJ, Leonardi MS, Berón Vera B, Vales DG, Ameghino S, Raga JA, periods on platforms, riverside piers, and around the local fish Crespo EA (2009) Population dynamics of Antarctophthirus microchir (Anoplura : Echinophthiriidae) in pups from South market lying in close contact to each other, which might in- American sea lion, Otaria flavescens, in Northern . crease the chance of horizontal lice transmission. Overall, the Parasitology 136:293–303 current data indicate that adult O. flavescens males might play Cárdenas-Alayza S (2017) South American sea lion (Otaria byronia). 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